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Advances in the Floral Structural Characterization of the Major Subclades of Malpighiales, One of the Largest Orders of Flowering Plants

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Advances in the Floral Structural Characterization of the Major Subclades of Malpighiales, One of the Largest Orders of Flowering Plants Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2013 Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants Endress, Peter K ; Davis, Charles C ; Matthews, Merran L DOI: https://doi.org/10.1093/aob/mct056 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-78190 Journal Article Published Version Originally published at: Endress, Peter K; Davis, Charles C; Matthews, Merran L (2013). Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants. Annals of Botany, 111(5):969-985. DOI: https://doi.org/10.1093/aob/mct056 Annals of Botany 111: 969–985, 2013 doi:10.1093/aob/mct056, available online at www.aob.oxfordjournals.org Advances in the floral structural characterization of the major subclades of Malpighiales, one of the largest orders of flowering plants Peter K. Endress1,*, Charles C. Davis2 and Merran L. Matthews1 1Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland and 2Department of Organismic and Evolutionary Biology, Harvard University Herbaria, 22 Divinity Avenue, Cambridge, MA 02138, USA * For correspondence. E-mail [email protected] Received: 28 November 2012 Revision requested: 21 December 2012 Accepted: 24 January 2013 Published electronically: 13 March 2013 † Background and Aims Malpighiales are one of the largest angiosperm orders and have undergone radical sys- tematic restructuring based on molecular phylogenetic studies. The clade has been recalcitrant to molecular Downloaded from phylogenetic reconstruction, but has become much more resolved at the suprafamilial level. It now contains so many newly identified clades that there is an urgent need for comparative studies to understand their structure, biology and evolution. This is especially true because the order contains a disproportionally large diversity of rain forest species and includes numerous agriculturally important plants. This study is a first broad systematic step in this endeavour. It focuses on a comparative structural overview of the flowers across all recently identified supra- familial clades of Malpighiales, and points towards areas that desperately need attention. http://aob.oxfordjournals.org/ † Methods The phylogenetic comparative analysis of floral structure for the order is based on our previously pub- lished studies on four suprafamilial clades of Malpighiales, including also four related rosid orders (Celastrales, Crossosomatales, Cucurbitales, Oxalidales). In addition, the results are compiled from a survey of over 3000 pub- lications on macrosystematics, floral structure and embryology across all orders of the core eudicots. † Key Results Most new suprafamilial clades within Malpighiales are well supported by floral structural features. Inner morphological structures of the gynoecium (i.e. stigmatic lobes, inner shape of the locules, placentation, presence of obturators) and ovules (i.e. structure of the nucellus, thickness of the integuments, presence of vas- cular bundles in the integuments, presence of an endothelium in the inner integument) appear to be especially suitable for characterizing suprafamilial clades within Malpighiales. at Universitaet Zuerich on April 20, 2013 † Conclusions Although the current phylogenetic reconstruction of Malpighiales is much improved compared with earlier versions, it is incomplete, and further focused phylogenetic and morphological studies are needed. Once all major subclades of Malpighiales are elucidated, more in-depth studies on promising structural features can be conducted. In addition, once the phylogenetic tree of Malpighiales, including closely related orders, is more fully resolved, character optimization studies will be possible to reconstruct evolution of structural and biological features within the order. Key words: Androecium, Celastrales, COM clade, core eudicots, evolution, floral structure, gynoecium, Malpighiales, ovules, Oxalidales, phylogeny, rosids. INTRODUCTION include Samydaceae and Scyphostegiaceae; Passifloraceae to also include Turneraceae and Malesherbiaceae), and new The eudicot order Malpighiales contains approx. 40 families suprafamilial clades of families have been discovered (e.g. and includes more than 16 000 species, making it one of the the parietal clade, the rhizophoroid clade and largest orders of the flowering plants (APG III, 2009; Rafflesiaceae + Euphorbiaceae; Schwarzbach and Ricklefs, Wurdack and Davis, 2009; Xi et al., 2012). The sheer morpho- 2000; Zhang and Simmons, 2006; Alford, 2007; Davis et al., logial diversity in the group, including such extremes as trop- 2007; Wurdack and Davis, 2009; Xi et al., 2012). Despite ical holoparasites with giant flowers and temperate trees and the extreme difficulty in resolving the order (Davis et al., herbs with tiny, simple flowers, has long made its classification 2005; Korotkova et al., 2009; Wurdack and Davis, 2009), challenging. First taking shape in the early 1990s (Chase et al., however, recent attempts using phylogenomic approaches 1993; APG I, 1998; Nandi et al., 1998), Malpighiales have have made significant progress, although some relationships undergone massive restructuring over the past 15 years as a remain unresolved (Wurdack and Davis, 2009; Xi et al., result of the molecular phylogenetic revolution (Savolainen 2012). In the most recent study by Xi et al. (2012) the 16 pre- et al., 2000a, b; Soltis et al., 2000; Davis and Chase, 2004; viously identified clades of Malpighiales, eight of which are APG III, 2009; Wurdack and Davis, 2009; Xi et al., 2012). suprafamilial (Wurdack and Davis, 2009), have been resolved A number of new families have been recognized (e.g. into three large clades. Nine additional suprafamilial subclades Peraceae, Centroplacaceae), others excluded (e.g. have also been resolved within these three major clades. A new Medusandraceae, Peridiscaceae), some traditional families phylogenetic analysis of Malpighiales based on structural fea- have been alternatively circumscribed (e.g. Salicaceae to also tures at a more refined level is our ultimate goal but will only # The Author 2013. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 970 Endress et al. — Floral structure and systematics in Malpighiales be possible to achieve once all families or suprafamilial clades appropriate taxon selection to elucidate putative synapo- have been equally studied. This endeavour will be of interest morphies for major Malpighiales subclades, and second, as especially for the evaluation of fossil Malpighiales, for we outline below in greater detail, numerous groups within which DNA is unavailable. In combination with molecular Malpighiales still lack sampling for morphological and ana- analyses it may also improve the phylogenetic resolution of tomical features. To rectify this, the laboratory of P.K.E. has the group as has been shown in other studies (Nandi et al., been conducting a series of comparative floral structural 1998; Doyle and Endress, 2000). studies focusing on several newly identified Malpighiales These newly recognized Malpighiales subclades provide a clades (Endress and Matthews, 2006b, 2012; Matthews and foundation for conducting a comprehensive comparative ana- Endress, 2008, 2011, 2013; Matthews et al., 2012). This re- lysis of their floral structure and biology, which to date has search programme has also included the closest relatives of been sorely lacking. The reason for this vacuum in our knowl- Malpighiales, Oxalidales and Celastrales (Matthews et al., edge is two-fold. First, the poor phylogenetic resolution (in- 2001; Matthews and Endress, 2002, 2005a), plus two addition- cluding sparse taxon sampling) within the order has hindered al rosid orders, Cucurbitales and Crossosomatales (Matthews and Endress, 2004, 2005b). The main aim of this research has been to identify special floral features that characterize these clades based on the reconstruction of their outer and Downloaded from TABLE 1. List of families in Malpighiales (following Xi et al., inner morphological surfaces using serial microtome sections 2012) plus scanning electron microscopy, and also anatomical and histological features. Concurrently, we have conducted a vast Achariaceae (16/12) literature survey including over 3000 publications on macro- Balanopaceae (1/1) systematics, reproductive structure and embryology throughout Bonnetiaceae (3/1) http://aob.oxfordjournals.org/ Calophyllaceae (4/1) all families of the core eudicots, which we have also used here. Caryocaraceae (3/0) To demonstrate the unbalanced sampling of structural fea- Centroplacaceae (0/0) tures for Malpighiales we prepared a table (Table 1) listing Chrysobalanaceae (9/1) the number of publications on aspects of ovule, embryo sac Clusiaceae (20/6) Ctenolophonaceae (5/0) and floral development as well as the inner floral structure Dichapetalaceae (4/1) for each family of Malpighiales [clade circumscription sensu Elatinaceae (6/6) Wurdack and Davis (2009) and Xi et al. (2012)]. The clades Erythroxylaceae (12/8) treated in these two papers were chosen over the APG III Euphorbiaceae (172/132) Euphroniaceae (1/0) (2009) list as they provide a more extensive representation of at Universitaet Zuerich on April 20, 2013
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